Reproduction of Marine Life, Birth of New Life! Investigating the Mysteries of Reproduction A primer on shark reproduction for aquarists Jose I. Castro NOAA, Southeast Fisheries Science Center, 75 Virginia Beach Drive, Miami, Florida 33149, USA Contact e-mail: [email protected] Introduction Aquariums are one of the most popular and profitable public entertainment enterprises, and sharks are invariably one of their most popular and prized exhibits. Unfortunately, due to a variety or reasons, sharks are among the most difficult species to maintain in captivity. Only a few species can be maintained for long periods and even fewer reproduce in captivity. Some small catsharks have been maintained in aquaria for many successive generations, and a few large species, such as the sand tiger shark and the nurse shark can survive in captivity for decades. The larger species are generally difficult to maintain in captivity, and most survive in present day aquariums only for short periods of days or weeks, or at best a few months. The goal of most aquarists, and the final test of successful aquarium husbandry, is to provide a captive environment where a species can attain its full life span and reproduce successfully, engendering successive captive generations. The purpose of this paper is to provide a primer on shark reproduction for aquarists, to help in understanding the reproductive processes of the sharks they keep and to provide a framework for aquarists to make observations that will contribute to our understanding of the reproductive biology of sharks. Because of the difficulties of studying and observing sharks in the natural environment, much can be learned in the aquarium, and aquarists can contribute significantly to our knowledge of sharks when their observations are systematically recorded and subsequently published. In the course of their long evolution, sharks evolved different reproductive adaptations that enhance the survival of their offspring. The first of these adaptations is internal fertilization. In animals with internal fertilization, the male transfers its sperm to the female, and fertilization occurs inside the female's body, so it is said to be internal. In male sharks, the pelvic fins are modified into stout, tube-like copulatory organs known as claspers, which are inserted into the female during copulation to transfer sperm. The clasper tip is armed with hooks or claws and it expands when inserted into the female, effectively attaching the male, hence the name "claspers". All sharks have internal fertilization, and their embryos spend their most vulnerable stages protected inside their mother’s womb, and thus their survival is enhanced. By contrast, fishes with external fertilization cast hundreds of thousand of gametes into the waters where they suffer heavy mortality. In addition to internal fertilization, sharks evolved diverse reproductive modes of nourishing their young to relatively large size. Most sharks produce small numbers of relatively large young that hatch or are born fully developed, looking like miniature copies of the adults. These young may reach as much as 25-30 % of the length of the mother. By being born at a relatively large size, the young sharks encounter fewer predators and have more available prey, thus enhancing their chances of survival. The production large Castro: A primer on shark reproduction for aquarists 52 Reproduction of Marine Life, Birth of New Life! Investigating the Mysteries of Reproduction young requires that large amounts of nutrients be available to nurture the embryo to large size, and sharks have evolved various modes of transferring nutrients to the young. These will be discussed below. Another adaptation of sharks which enhances the survival of their young is the use of nursery areas. These are specific areas of high productivity where the females travel to give birth and where the young encounter few predators and an abundance of small prey (Castro, 1993). The reproductive modes of sharks have been traditionally grouped into two major categories: oviparity (egg laying) and viviparity (giving birth to live young). In turn, viviparous sharks can be divided into several groups, depending on their mode of nourishing their embryos to large size. The different forms of viviparity have been the subject of various classifications (For reviews see Wourms, 1977; Hamlett and Koob, 1999; Conrath and Musick, 2012). None of these is completely satisfactory because there are so many adaptations and because we know so little about the maternal-embryonic processes of sharks. It is not the author’s purpose here to propose a new classification of the modes of reproduction in sharks, nor is it to demonstrate all the variations of viviparity in sharks. The purpose of this paper is to provide a simple primer to be used by aquarists and others to understand some of the reproductive processes of some the sharks they encounter in their work or investigations. Much remains to be learned about the reproductive processes of sharks and aquarists can contribute much to that endeavor. Oviparity The most primitive mode of reproduction in sharks is oviparity or egg laying. This is a modified oviparity, different to that of bony fishes. Oviparous sharks lay large eggs that contain sufficient yolk to nourish the embryo through development, and allow it to emerge as a fully developed miniature shark. By contrast, the eggs of most bony fishes are relatively minute and contain only a small amount of yolk. The small amount of nutrients in the egg can only support the developing embryo for a short time, and thus the embryo hatches out as a larva that usually bears little resemblance to the adult. Both eggs and larvae are highly vulnerable to biotic factors and predators for prolonged periods of time and consequently suffer heavy mortality. Oviparity in sharks is primarily confined to three families: the Scyliorhinidae, the Orectolobidae, and the Heterodontidae. The evolution of shark oviparity and the production of a small young that hatch at a relatively large size has contributed to the evolutionary success of sharks. The eggs of oviparous sharks are enclosed in leathery cases that are deposited on the bottom without any further contact with the parent. These egg cases are usually rectangular of conical and have adhesive tendrils used for attachment to bottom structures (Figure 1). The embryos hatch out after some months or a year, depending on water temperature. The hatchlings of oviparous sharks are very small in comparison to the mother's size, because the embryos have only that amount of yolk in the egg case to nurture them through development. The chain dogfish (Scyliorhinus retifer), a species common in the continental slope of eastern North America, is an example of an oviparous shark that has been studied in the aquarium (Castro et al., 1988), and its reproductive biology will be briefly summarized here. Castro: A primer on shark reproduction for aquarists 53 Reproduction of Marine Life, Birth of New Life! Investigating the Mysteries of Reproduction Figure 1. Chain dogfish egg case. Note adhesive tendrils on each corner of the egg case. Courtship begins as male and a female swim together almost constantly, often in slow, tight circles near the bottom, with the male often biting the female. When the sharks are ready to mate, the male bites the female near the tail and proceeds to move it bite forward. The female may struggle at first but soon becomes listless. The male moves its bite anteriorly along the flanks and eventually grabs the pectoral fin or the axilla. When firmly attached to the pectoral fin or area, the male then curls it body around the female, inserts a clasper and copulation is accomplished. After a short while the two sharks swim apart. In the natural environment as well as in the aquarium, chain dogfish females use vertical bottom structures to attach their eggs. When a female is ready to lay her eggs, the long adhesive tendrils at each corner of the egg case protrude through the cloaca and trail behind the shark. The female then locates a vertical structure (a coral, a sponge, or any solid structure) and begins to swim tight circles around the structure, causing the trailing tendrils to adhere to the structure (Figure 2). Once the tendrils are firmly attached to the structure, Figure 2. Chain dogfish females attaching egg cases to upright structure. the female speeds up her circling, and this causes the egg case to be physically pulled from the cloaca. Females usually ovulate their oocytes in pairs. The interval between successive pairs is about two weeks. The interval between the deposition of the first egg case of a pair and the second ranges from a few minutes to a few days, with the longest interval observed being 8 days. Each female produces egg cases of consistent size and coloration, thus an aquarist can usually determine which female may have produce a Castro: A primer on shark reproduction for aquarists 54 Reproduction of Marine Life, Birth of New Life! Investigating the Mysteries of Reproduction given egg cases in a tank of several females. In the wild, structures suitable for egg attachment may be scarce, and many females in one area may use the same structure, creating large masses of egg cases with embryos in many different stages. Whether this is done because of the scarcity of suitable structures or whether the eggs derive some protection from the clustering is unknown. The egg cases have small slits that open enzymatically after the embryo reaches a given size (Figure 3). These slits serve to aerate the egg case, and the embryo constantly fans its tail for this purpose. Embryo development is temperature dependent and in the case of the chain dogfish average development time was 256 days at water temperatures of 11.7–12.8ºC, and hatching occurred when embryos reached 10–11 cm.